Leaf Energy Balance Requires Mitochondrial Respiration and Export of Chloroplast NADPH in the Light

Abstract

Key aspects of leaf mitochondrial metabolism in the light remain unresolved. For example, there is debate about the relative importance of exporting reducing equivalents from mitochondria for the peroxisomal steps of photorespiration versus oxidation of NADH to generate ATP by oxidative phosphorylation. Here, we address this and explore energetic coupling between organelles in the light using a diel flux balance analysis model. The model included more than 600 reactions of central metabolism with full stoichiometric accounting of energy production and consumption. Different scenarios of energy availability (light intensity) and demand (source leaf versus a growing leaf) were considered, and the model was constrained by the nonlinear relationship between light and CO 2 assimilation rate. The analysis demonstrated that the chloroplast can theoretically generate sufficient ATP to satisfy the energy requirements of the rest of the cell in addition to its own. However, this requires unrealistic high light use efficiency and, in practice, the availability of chloroplast-derived ATP is limited by chloroplast energy dissipation systems, such as nonphotochemical quenching, and the capacity of the chloroplast ATP export shuttles. Given these limitations, substantial mitochondrial ATP synthesis is required to fulfill cytosolic ATP requirements, with only minimal, or zero, export of mitochondrial reducing equivalents. The analysis also revealed the importance of exporting reducing equivalents from chloroplasts to sustain photorespiration. Hence, the chloroplast malate valve and triose phosphate-3-phosphoglycerate shuttle are predicted to have important metabolic roles, in addition to their more commonly discussed contribution to the avoidance of photooxidative stress.

Atomic structure of a mitochondrial complex I intermediate from vascular plants

“…Mitochondrial respiration is the major source of ATP in plants’ non-photosynthetic tissues such as roots. In photosynthetic tissue in the light, the role of mitochondrial respiration in ATP production is debated ( Shameer et al, 2019 ; Gardeström and Igamberdiev, 2016 ) (see Appendix). Moreover, in photosynthetic tissue, conditions of intense light may lead to an over-production of reducing equivalents (NAD(P)H), which could be detrimental to the cells via the production of reactive oxygen species (ROS).…”

Flexibility in the Energy Balancing Network of Photosynthesis Enables Safe Operation under Changing Environmental Conditions

“…Flux balance analysis of photosynthetic systems that are optimized for energy production per photon of absorbed light predict the malate valve to be the optimal mechanism of energy balancing unless the additional costs of enzymatic interconversions are introduced into the model [105]. This is also supported in work using a modified flux balance analysis approach, which weights flux solutions based on pathway complexity [106]. As light intensity increases, absorbed light energy is actively released as NPQ, indicating that under high light, the system is no longer light limited and the energy balancing network could trade the more light-optimal malate valve for CEF.…”

In planta study of photosynthesis and photorespiration using NADPH and NADH/NAD+ fluorescent protein sensors

“…Experimental data obtained from barley leaf protoplasts 23,24,26 and isolated mitochondria 27 suggest that photorespiration is the major source of reducing equivalents to the mETC. However, this has not been examined in a whole plant level, and the direction of the flow of reducing equivalents between different subcellular compartments during photosynthesis has not yet been fully resolved 28 .…”